Apomixis is a form of asexual reproduction in which seeds are formed without fertilization. Draba oligosperma Hook. (Brassicaceae) is a North American Cordilleran and predominantly apomictic species that was shown to produce sexual seed at a low-level (3%) throughout its geographic range. Previous phylogenetic analyses of Draba L. globally established that it is a young, hybridizing, polyploid, and highly diversifying genus of ~400 taxa. Here we provide an updated time-calibrated phylogeny with a portion of North American Cordilleran species using newly targeted intronic regions and present a hypothetical origin of D. oligosperma based on extensive population genetic sampling and ddRADtag sequencing. The migration patterns inferred from these data suggest lineages were isolated in the high mountains of Wyoming, Montana, and Idaho, and spread east, north, and westward from there. This is one of the first large scale population-level studies that clarifies dispersal histories of lineages across the Intermountain region of the Great Basin from Nevada to the Sierra, Carson, and White ranges of California. Further exploration of the migration patterns of this species and the role of apomixis during population establishment will be discussed.